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The entry of cucumber mosaic virus into cucumber xylem is facilitated by co-infection with zucchini yellow mosaic virus

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Abstract

We investigated the synergistic effects of co-infection by zucchini yellow mosaic virus (ZYMV) and cucumber mosaic virus (CMV) on viral distribution in the vascular tissues of cucumber. Immunohistochemical observations indicated that ZYMV was present in both the phloem and xylem tissues. ZYMV-RNA was detected in both the xylem wash and guttation fluid of ZYMV-inoculated cucumber. Steam treatment at a stem internode indicated that ZYMV enters the xylem vessels and moves through them but does not cause systemic infection in the plant. CMV distribution in singly infected cucumbers was restricted to phloem tissue. By contrast, CMV was detected in the xylem tissue of cotyledons in plants co-infected with CMV and ZYMV. Although both ZYMV-RNA and CMV-RNA were detected in the xylem wash and upper internodes of steam-treated, co-infected cucumbers grown at 24 °C, neither virus was detected in the upper leaves using an ELISA assay. Genetically modified CMV harboring the ZYMV HC-Pro gene was distributed in the xylem and phloem tissues of singly inoculated cucumber cotyledons. These results indicate that the ZYMV HC-Pro gene facilitates CMV entry into the xylem vessels of co-infected cucumbers.

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References

  1. Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA 95:13079–13084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Barker H, McGeachy KD, Ryabov EV, Commandeur U, Mayo MA, Taliansky M (2001) Evidence for RNA-mediated defense effects on the accumulation of Potato leafroll virus. J Gen Virol 82:3099–3106

    Article  CAS  PubMed  Google Scholar 

  3. Betti C, Lico C, Maffi D, D’Angeli S, Altamura MM, Benvenuto E, Faoro F, Baschieri S (2012) Potato virus X movement in Nicotiana benthamiana: new details revealed by chimeric coat protein variants. Mol Plant Pathol 13:198–203

    Article  CAS  PubMed  Google Scholar 

  4. Calvert LA, Ghabrial SA (1983) Enhancement by soybean mosaic virus of bean pod mottle virus titer in doubly infected soybean. Phytopathology 73:992–997

    Article  Google Scholar 

  5. Chambers TC, Francki RI (1966) Localization and recovery of lettuce necrotic yellows virus from xylem tissues of Nicotiana glutinosa. Virology 29:673–676

    Article  CAS  PubMed  Google Scholar 

  6. Choi SK, Yoon JY, Ryu KH, Choi JK, Palukaitis P, Park WM (2002) Systemic movement of a movement-deficient strain of Cucumber mosaic virus in zucchini squash is facilitated by a cucurbitinfecting potyvirus. J Gen Virol 83:3173–3178

    Article  CAS  PubMed  Google Scholar 

  7. Ding XS, Carter SA, Deom CM, Nelson RS (1998) Tobamovirus and potyvirus accumulation in minor veins of inoculated leaves from representatives of the Solanaceae and Fabaceae. Plant Physiol 116:125–136

    Article  CAS  Google Scholar 

  8. Ding XS, Flasinski S, Nelson RS (1999) Infection of barley by brome mosaic virus is restricted predominantly to cells in and associated with veins through a temperature-dependent mechanism. Mol Plant Microbe Interact 12:615–623

    Article  CAS  Google Scholar 

  9. Ding XS, Boydston CM, Nelson RS (2001) Presence of Brome mosaic virus in barley guttation fluid and its association with localized cell death response. Phytopathology 91:440–448

    Article  CAS  PubMed  Google Scholar 

  10. Dubois F, Sangwan RS, Sangwan-Norreel BS (1994) Spread of Beet necrotic yellow vein virus in infected seedlings and plants of sugar beet (Beta vulgaris). Protoplasma 179:72–82

    Article  Google Scholar 

  11. French CJ, Elder M (1999) Virus particles in guttate and xylem of infected cucumber (Cucumis sativus L.). Ann Appl Biol 134:81–87

    Article  Google Scholar 

  12. Glais L, Tribodet M, Kerlan C (2002) Genomic variability in Potato potyvirus Y (PVY): evidence that PVYNW and PVYNTN variants are single to multiple recombinants between PVYO and PVYN isolates. Arch Virol 147:363–378

    Article  CAS  PubMed  Google Scholar 

  13. Goldberg K-B, Brakke MK (1987) Concentration of maize chlorotic mottle virus is increased in mixed infections with maize dwarf mosaic virus, strain B. Phytopathology 77:162–167

    Article  Google Scholar 

  14. González-Jara P, Atencio FA, Martínez-García B, Barajas D, Tenllado F, Díaz-Ruíz JR (2005) A single amino acid mutation in the Plum pox virus helper component-proteinase gene abolishes both synergistic and RNA silencing suppression activities. Phytopathology 95:894–901

    Article  PubMed  Google Scholar 

  15. Guerini MN, Murphy JF (1999) Resistance of Capsicum annuum ‘Avelar’ to pepper mottle potyvirus and alleviation of this resistance by co-infection with cucumber mosaic cucumovirus are associated with virus movement. J Gen Virol 80:2785–2792

    Article  CAS  PubMed  Google Scholar 

  16. Hacker DL, Fowler BC (2000) Complementation of the host range restriction of southern cowpea mosaic virus in bean by southern bean mosaic virus. Virology 266:140–149

    Article  CAS  PubMed  Google Scholar 

  17. Hull R (2014) Plant Virol, 5th edn. Academic Press, San Diego

    Google Scholar 

  18. Kasschau KD, Carrington JC (1998) A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95:461–470

    Article  CAS  PubMed  Google Scholar 

  19. Kosaka Y, Fukunishi T (1997) Multiple inoculation with three attenuated viruses for the control of cucumber virus disease. Plant Dis 81:733–738

    Article  Google Scholar 

  20. Malyshenko SI, Kondakova OA, Taliansky ME, Atabekov JG (1989) Plant virus transport function: complementation by helper viruses is non-specific. J Gen Virol 70:2751–2757

    Article  Google Scholar 

  21. Manabayeva SA, Shamekova M, Park JW, Ding XS, Nelson RS, Hsieh YC, Omarov RT, Scholthof HB (2013) Differential requirements for Tombusvirus coat protein and P19 in plants following leaf versus root inoculation. Virology 439:89–96

    Article  CAS  PubMed  Google Scholar 

  22. Mochizuki T, Hirai K, Kanda A, Ohnishi J, Ohki T, Tsuda S (2009) Induction of necrosis via mitotochondrial targeting of Melon necrotic spot virus replication protein p29 by its second transmembrane domain. Virology 390:239–249

    Article  CAS  PubMed  Google Scholar 

  23. Moreno IM, Thompson JR, García-Arenal F (2004) Analysis of the systemic colonization of cucumber plants by Cucumber green mottle mosaic virus. J Gen Virol 85:749–759

    Article  CAS  PubMed  Google Scholar 

  24. Opalka N, Brugidou C, Bonneau C, Nicole M, Beachy RN, Yeager M, Fauquet C (1998) Movement of rice yellow mottle virus between xylem cells through pit membranes. Proc Natl Acad Sci USA 95:3323–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Poolpol P, Inouye T (1986) Enhancement of cucumber mosaic virus multiplication by zucchini yellow mosaic virus in doubly infected cucumber plants. Ann Phytopathol Soc Japan 52:22–30

    Article  Google Scholar 

  26. Pruss G, Ge X, Shi XM, Carrington JC, Vance VB (1997) Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rochow WF, Ross AF (1955) Virus multiplication in plants doubly infected by potato viruses X and Y. Virology 1:10–27

    Article  CAS  PubMed  Google Scholar 

  28. Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237:283–295

    Article  CAS  PubMed  Google Scholar 

  29. Ryang B-S, Kobori T, Matsumoto T, Kosaka Y, Ohki ST (2004) Cucumber mosaic virus 2b protein compensates for restricted systemic spread of Potato virus Y in doubly infected tobacco. J Gen Virol 85:3405–3414

    Article  CAS  PubMed  Google Scholar 

  30. Ryang B-S, Matsumoto T, Kobori T, Kosaka Y, Ohki ST (2005) 2b Protein is essential to induce a novel gradual cell death in Zucchini yellow mosaic virus-inoculated cucumber cotyledon co-infected with Cucumber mosaic virus. J Gen Plant Pathol 71:308–313

    Article  CAS  Google Scholar 

  31. Sáenz P, Quiot L, Quiot JB, Candresse T, García JA (2001) Pathogenicity determinants in the complex virus population of a Plum pox virus isolate. Mol Plant Microbe Interact 14:278–287

    Article  PubMed  Google Scholar 

  32. Saitoh H, Fujiwara M, Ohki ST, Osaki T (1999) The coat protein gene is essential for the systemic infection of Cucumber mosaic virus in Cucumis figarei at high temperature. Ann Phytopathol Soc Japan 65:248–253

    Article  CAS  Google Scholar 

  33. Savenkov EI, Valkonen JP (2001) Potyviral helper-component proteinase expressed in transgenic plants enhances titers of Potato leaf roll virus but does not alleviate its phloem limitation. Virology 283:285–293

    Article  CAS  PubMed  Google Scholar 

  34. Schneider IR, Worley JF (1959) Upward and downward transport of infectious particles of southern bean mosaic virus through steamed portions of bean stems. Virology 8:230–242

    Article  CAS  PubMed  Google Scholar 

  35. Shi XM, Miller H, Verchot J, Carrington JC, Vance VB (1997) Mutations in the region encoding the central domain of helper component-proteinase (HC-Pro) eliminate potato virus X/potyviral synergism. Virology 231:35–42

    Article  CAS  PubMed  Google Scholar 

  36. Takeshita M, Takanami Y (2000) Defective long-distance transport of Cucumber mosaic virus in radish is efficiently complemented by Turnip mosaic virus. J Gen Plant Pathol 66:254–257

    Article  Google Scholar 

  37. Thompson JR, García-Arenal F (1998) The bundle sheath-phloem interface of Cucumis sativus is a boundary to systemic infection by tomato aspermy virus. Mol Plant Microbe Interact 11:109–114

    Article  CAS  Google Scholar 

  38. Tribodet M, Glais L, Kerlan C, Jacquot E (2005) Characterization of Potato virus Y (PVY) molecular determinants involved in the vein necrosis symptom induced by PVYN isolates in infected Nicotiana tabacum cv. Xanthi. J Gen Virol 86:2101–2105

    Article  CAS  PubMed  Google Scholar 

  39. Vance VB (1991) Replication of potato virus X RNA is altered in coinfections with potato virus Y. Virology 182:486–494

    Article  CAS  PubMed  Google Scholar 

  40. Vance VB, Berger PH, Carrington JC, Hunt AG, Shi XM (1995) 5’ proximal potyviral sequences mediate potato virus X/potyviral synergistic disease in transgenic tobacco. Virology 206:583–590

    Article  CAS  PubMed  Google Scholar 

  41. Verchot J, Driskel BA, Zhu Y, Hunger RM, Littlefield LJ (2001) Evidence that soilborne wheat mosaic virus moves long distance through the xylem in wheat. Protoplasma 218:57–66

    Article  CAS  PubMed  Google Scholar 

  42. Wan J, Cabanillas DG, Zheng H, Laliberté JF (2015) Turnip mosaic virus moves systemically through both phloem and xylem as membrane-associated complexes. Plant Physiol 167:1374–1388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang HL, Wang Y, Giesman-Cookmeyer D, Lommel SA, Lucas WJ (1998) Mutations in viral movement protein alter systemic infection and identify an intercellular barrier to entry into the phloem long-distance transport system. Virology 245:75–89

    Article  CAS  PubMed  Google Scholar 

  44. Wang Y, Lee KC, Gaba V, Wong SM, Palukaitis P, Gal-On A (2004) Breakage of resistance to Cucumber mosaic virus by co-infection with Zucchini yellow mosaic virus: enhancement of CMV accumulation independent of symptom expression. Arch Virol 149:379–396

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-1, Gakuen-cho, Naka-ku, Sakai, Osaka, 599-8531, Japan

    Tomofumi Mochizuki, Shinya Nobuhara, Miho Nishimura, Masaki Naoe, Tadashi Matsumoto & Satoshi T. Ohki

  2. Kyoto Biken Laboratories Inc., Uji, Kyoto, 611-0041, Japan

    Bo-Song Ryang

  3. Kyoto Prefectural Agriculture, Forestry, and Fisheries Technology Center, Seika-cho, Kyoto, 619-0244, Japan

    Yoshitaka Kosaka

Authors
  1. Tomofumi Mochizuki
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  2. Shinya Nobuhara
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  3. Miho Nishimura
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  4. Bo-Song Ryang
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  7. Yoshitaka Kosaka
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  8. Satoshi T. Ohki
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Correspondence to Satoshi T. Ohki.

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705_2016_2970_MOESM1_ESM.tif

FIG. S1 Tissue immunoblot analysis of stem sections of cucumber plants inoculated with CMV alone or with CMV and ZYMV. Tissue prints for the detection of CMV at 3, 5, and 7 dpi. The locations of the sections are indicated by lines labeled (a) to (h). The positions of the tested internode sections are indicated on the right. Purple-stained areas show the distribution of CMV CP. Note that at 3 dpi, CMV CP was detected in almost all upper parts (d, e, f, and g) of doubly infected cucumber, while CMV CP was detected only in the stem below the inoculated leaf of singly infected cucumber. Tissue immunoblot analysis was carried out as described by Ryang et al. (2004). The cut surface of the stem was pressed directly onto nitrocellulose membranes (GE Healthcare, WI). The nitrocellulose membranes were incubated with a viral CP-specific primary antibody and an alkaline phosphatase-conjugated IgG and incubated in BCIP/NBT color substrate solution (Sigma, MO). (TIFF 13461 kb)

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Mochizuki, T., Nobuhara, S., Nishimura, M. et al. The entry of cucumber mosaic virus into cucumber xylem is facilitated by co-infection with zucchini yellow mosaic virus. Arch Virol 161, 2683–2692 (2016). https://doi.org/10.1007/s00705-016-2970-0

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  • DOI: https://doi.org/10.1007/s00705-016-2970-0

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